Associations of Enlarged Perivascular Spaces With Brain Lesions, Brain Age, and Clinical Outcomes in Chronic Traumatic Brain Injury.


Journal

Neurology
ISSN: 1526-632X
Titre abrégé: Neurology
Pays: United States
ID NLM: 0401060

Informations de publication

Date de publication:
04 07 2023
Historique:
received: 07 11 2022
accepted: 17 03 2023
pmc-release: 04 07 2024
medline: 5 7 2023
pubmed: 9 5 2023
entrez: 8 5 2023
Statut: ppublish

Résumé

Enlarged perivascular spaces (ePVS) have been identified as a key signature of glymphatic system dysfunction in neurologic conditions. The incidence and clinical implications of ePVS after traumatic brain injury (TBI) are not yet understood. We investigated whether individuals with chronic moderate-to-severe TBI had an increased burden of ePVS and whether ePVS burden is modulated by the presence of focal lesions, older brain age, and poorer sleep quality. We examined whether an increased burden of ePVS was associated with poorer cognitive and emotional outcomes. Using a cross-sectional design, participants with a single moderate-to-severe chronic TBI (sustained ≥10 years ago) were recruited from an inpatient rehabilitation program. Control participants were recruited from the community. Participants underwent 3T brain MRI, neuropsychological assessment, and clinical evaluations. ePVS burden in white matter was quantified using automated segmentation. The relationship between the number of ePVS, group membership, focal lesions, brain age, current sleep quality, and outcome was modeled using negative binomial and linear regressions. This study included 100 participants with TBI (70% male; mean age = 56.8 years) and 75 control participants (54.3% male; mean age = 59.8 years). The TBI group had a significantly greater burden of ePVS (prevalence ratio rate [PRR] = 1.29, TBI is associated with a greater burden of ePVS, especially when there have been bilateral brain lesions. ePVS was associated with reduced verbal memory performance. ePVS may indicate ongoing impairments in glymphatic system function in the chronic postinjury period.

Sections du résumé

BACKGROUND AND OBJECTIVES
Enlarged perivascular spaces (ePVS) have been identified as a key signature of glymphatic system dysfunction in neurologic conditions. The incidence and clinical implications of ePVS after traumatic brain injury (TBI) are not yet understood. We investigated whether individuals with chronic moderate-to-severe TBI had an increased burden of ePVS and whether ePVS burden is modulated by the presence of focal lesions, older brain age, and poorer sleep quality. We examined whether an increased burden of ePVS was associated with poorer cognitive and emotional outcomes.
METHODS
Using a cross-sectional design, participants with a single moderate-to-severe chronic TBI (sustained ≥10 years ago) were recruited from an inpatient rehabilitation program. Control participants were recruited from the community. Participants underwent 3T brain MRI, neuropsychological assessment, and clinical evaluations. ePVS burden in white matter was quantified using automated segmentation. The relationship between the number of ePVS, group membership, focal lesions, brain age, current sleep quality, and outcome was modeled using negative binomial and linear regressions.
RESULTS
This study included 100 participants with TBI (70% male; mean age = 56.8 years) and 75 control participants (54.3% male; mean age = 59.8 years). The TBI group had a significantly greater burden of ePVS (prevalence ratio rate [PRR] = 1.29,
DISCUSSION
TBI is associated with a greater burden of ePVS, especially when there have been bilateral brain lesions. ePVS was associated with reduced verbal memory performance. ePVS may indicate ongoing impairments in glymphatic system function in the chronic postinjury period.

Identifiants

pubmed: 37156615
pii: WNL.0000000000207370
doi: 10.1212/WNL.0000000000207370
pmc: PMC10351302
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e63-e73

Subventions

Organisme : NIA NIH HHS
ID : P30 AG066518
Pays : United States

Informations de copyright

© 2023 American Academy of Neurology.

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Auteurs

Amelia J Hicks (AJ)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia.

Benjamin Sinclair (B)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia.

Sandy R Shultz (SR)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia.

William Pham (W)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia.

Lisa C Silbert (LC)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia.

Daniel L Schwartz (DL)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia.

Christopher C Rowe (CC)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia.

Jennie L Ponsford (JL)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia.

Meng Law (M)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia.

Gershon Spitz (G)

From the Monash-Epworth Rehabilitation Research Centre (A.J.H., J.L.P., G.S.), Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Department of Neuroscience (A.J.H., B.S., S.R.S., W.P., M.L., G.S.), Central Clinical School, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton; Department of Neurology (B.S.), Alfred Health, Melbourne, Australia; Health and Human Services (S.S.), Vancouver Island University, Nanaimo; Division of Medical Sciences (S.S.), University of Victoria, British Columbia, Canada; NIA-Layton Oregon Aging & Alzheimer's Disease Research Center (L.C.S., D.L.S.), Oregon Health & Science University; Department of Neurology (L.C.S.), Portland Veterans Affairs Health Care System; Advanced Imaging Research Center (D.L.S.), Oregon Health & Science University, Portland; Department of Molecular Imaging and Therapy (C.C.R.), Austin Health, Heidelberg; Florey Department of Neuroscience and Mental Health (C.C.R.), University of Melbourne, Parkville; and Department of Radiology (M.L.), Alfred Health, Melbourne, Australia. gershon.spitz@monash.edu.

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